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Biol. Rev. (2020), pp. 000–000. 1 doi: 10.1111/brv.12612 Camouflage in predators

Matilda Q. R. Pembury Smith* and Graeme D. Ruxton School of , University of St Andrews, Dyers Brae House, St Andrews, Fife, KY16 9TH, U.K.

ABSTRACT

Camouflage – that prevent detection and/or recognition – is a key example of by , making it a primary focus in evolutionary and behaviour. Most work has focused on camouflage as an anti-predator . However, predators also display specific colours, patterns and behaviours that reduce visual detection or recognition to facilitate . To date, very little attention has been given to predatory camouflage strategies. Although many of the same principles of camouflage studied in prey translate to predators, differences between the two groups (in motility, relative size, and control over the time and place of predation attempts) may alter selection pressures for certain visual and behavioural traits. This makes many predatory camouflage techniques unique and rarely documented. Recently, new technologies have emerged that provide a greater opportunity to carry out research on natural predator–prey interactions. Here we review work on the camouflage strategies used by pursuit and ambush predators to evade detection and recognition by prey, as well as looking at how work on prey camouflage can be applied to predators in order to understand how and why specific predatory camouflage strategies may have evolved. We highlight that a shift is needed in camouflage research focus, as this field has comparatively neglected cam- ouflage in predators, and offer suggestions for future work that would help to improve our understanding of camouflage.

Key words: camouflage, , predation, behaviour, movement, , evolution

CONTENTS I. Introduction ...... 2 II. Ambush predators ...... 2 (1) Aggressive crypsis ...... 3 (2) Aggressive masquerade ...... 4 (3) ...... 4 (a) Aggressive mimicry without a lure ...... 4 (b) Aggressive mimicry using a generalised lure ...... 5 (c) Aggressive mimicry using a specialised lure ...... 5 III. Pursuit predators ...... 6 (1) Dynamic crypsis via background-matching ...... 6 (2) Dynamic crypsis via disruptive colouration ...... 6 (3) Motion masquerade ...... 7 (4) Motion camouflage ...... 8 IV. Factors affecting the evolution of camouflage strategies in predators ...... 9 (1) Time of attack ...... 9 (2) Size ...... 10 (3) Prey ...... 10 (4) Environment ...... 12 V. Conclusions ...... 12 VI. References ...... 13

* Address for correspondence (Tel: +44 (0) 7503152203; E-mail: [email protected])

Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and in any medium, provided the original work is properly cited. 2 Matilda Q. R. Pembury Smith and Graeme D. Ruxton

I. INTRODUCTION arise are key examples of evolution by natural selection (Wallace, 1889; Poulton, 1890; Cott, 1940), camouflage as an Animal camouflage is a morphological adaptation which anti-predator strategy is heavily documented in the literature. describes all forms of concealment that hinder detection Many predators also display specific colours, patterns and and recognition (Merilaita & Stevens, 2011). Predation, a behaviours that appear to reduce visual detection or recognition in which one organism kills another to improve prey-capture success. Although some predator sys- for food, is likely to be one of the strongest selective forces tems have been analysed, less attention has been given overall in . Camouflage is often considered a critical compo- to predatory camouflage strategies, likely a result of increased nent of both prey and predator survival strategies challenges when monitoring predatory behaviour. The terri- (Cott, 1940; Endler, 1981; Stevens & Merilaita, 2009; Rux- tories of large predators span wide geographical areas, making ton, Sherratt & Speed, 2004). observations of natural predation events difficult, and their large Although camouflage is used as an umbrella term to describe size means handling can impose a risk to the investigator. Most all strategies that prevent detection and recognition, there are predation events are hard to predict, as some predatory strate- many different ways in which organisms can conceal them- gies are only expressed at the onset of an attack. It can also be selves. The most commonly documented is crypsis: adaptations difficult to identify whether a particular trait has evolved to involving body colouration that delay detection (Endler, 1978; reduce detection by prey or detection by another predator, as Merilaita & Stevens, 2011; Merilaita, Scott-Samuel & non-apex predators will operate under both selection pressures. Cuthill, 2017; Ruxton et al., 2004). There are many forms of Despite these challenges, camouflage in predators is important crypsis, the best known being background-matching whereby to document. Although many of the same principles studied in an organism matches the colour and pattern of their surround- prey, such as minimising detection and or recognition, also ings (Stuart-, Moussalli & Whiting, 2008; Merilaita & apply to predators, the purpose of camouflage in predators is Stevens, 2011; Ruxton & Stevens, 2015; Kang, Kim & to gain close proximity to prey. Pursuit and ambush predation Jang, 2016). Others include: disruptive colouration, where use different strategies to achieve this goal, giving rise to a vari- an organism displays a highly contrasting colour pattern in ety of unique adaptations. Predators are also generally larger order to break up their body outline (Cuthill et al., 2005; than their prey. Although research on the role of size on camou- Schaefer & Stobbe, 2006; Stevens & Cuthill, 2006); self- flage is limited, it has been established that larger organisms are shadow concealment (Wilkinson & Sherratt, 2008; Kelley & more conspicuous in comparison to small organisms Merilaita, 2015; Caro, 2016), in which colour patterns (nor- (Main, 1987), meaning that predators must evolve ways in mally a dark upper surface colour and a pale underside) which to remain camouflaged despite their size. Finally, as pred- reduce detection by subverting variation in shadowing that is ators are at liberty to choose when and where to attack their used to separate objects visually from their background prey, they only need to avoid detection during these specific (Chapman, Kaufman & Chapman, 1994; Stauffer, Hale & times and locations. By contrast, prey need to maintain Seltzer, 1999); transparency (Mackie & Mackie, 1967; camouflagemoreconsistentlyastheyhavealimitedabilityto Johnsen, 2001); silvering/mirrors (Denton, 1970, 1971) and predict the presence of a threat. This enables predators to self-decoration (Allgaier, 2007; Yanes et al., 2009). fine-tune their camouflage strategy to specific situations, unlike Despite camouflage research predominantly focusing on prey which have to achieve successful camouflage over a range the efficacy of crypsis strategies, there are many other forms of contexts. These differences between predators and prey may of camouflage that do not prevent initial detection. They alter the selection pressures for certain visual and behavioural instead interfere with an organism’s cognitive processes traits, making many predatory camouflage strategies unique. rather than sensory processes, in order to reduce recognition This review analyses anti-detection and anti-recognition or capture success. Examples include masquerade, in which strategies in ambush and pursuit predators, focusing on the the organism resembles another object (Endler, 1981; Allen & differences and similarities between the selection pressures Cooper, 1985; Edmunds, 1990; Skelhorn et al., 2010), dazzle they face, and how these contrast with those experienced by camouflage, in which detection occurs but colour patterns or prey. The diversity of camouflage strategies in predators movement confuse the detector as to the animal’s speed and highlights the importance of minimising detection by prey. direction (Thayer, 1909; Jackson, Ingram & Campbell, 1976; As some predatory taxa display camouflage strategies not Behrens, 1999; Stevens, Yule & Ruxton, 2008), and mimicry, observed in prey, a new focus on predators is warranted to in which one organism appears similar to another organism gain a greater understanding of how and why these traits in order to deceive an observer (Wickler, 1968; Edmunds, evolve and are selected for in predators. 1974; Smith & Harper, 1995). By adopting a mimetic pheno- type an organism will alter the selection pressures on the model they are mimicking. By contrast, masquerading organisms will have no effect on their model (Skelhorn, II. AMBUSH PREDATORS Rowland & Ruxton, 2009). As predator–prey relationships are a substantial compo- There has been extensive research on animal camouflage nent of all biological communities, and the adaptations that showing that the efficacy of mechanisms such as

Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Camouflage in predators 3 background-matching (Endler, 1981; Cuthill et al., 2005), evading its own predators, the resides in environments disruptive colouration, masquerade and self-shadowing that do not provide a background match (such as burrows (Ruxton et al., 2004), rely largely on the organism (and the and deadwood), suggesting that the background-matching background against which it is seen) remaining stationary evolved only to improve prey-capture success (Poulton, 1890; Cott, 1940; Heatwole, 1968; Zhang & (Loos et al., 2011). Richardson, 2007). Lower levels of activity in camouflaged In non-apex predators, crypsis strategies have two func- organisms decrease their probability of detection (Endler, tions: to allow sufficient proximity to the prey to enable a suc- 1978; Ioannou & Krause, 2009), with some authors even stat- cessful attack, and to reduce detection by their own ing that moving organisms cannot be camouflaged (Regan & predators. This dual can be seen in many species Beverley, 1984; Ioannou & Krause, 2009; Lui et al., 2012; of jumping (Oxford & Gillespie, 1998; Théry & Yin et al., 2015; Sokolov et al., 2018). Casas, 2002), which display clear specialisations in pheno- Ambush predators are organisms that ‘sit and wait’ until typic appearance according to their preferred environment mobile prey are within close proximity before they attack. (Cumming & Wesolowska, 2004). Robledo-Ospina- This predatory strategy minimises movement by the preda- et al. (2017) observed and compared cryptic strategies in tor, reducing the likelihood of detection by prey, and allows two genera of (Anasaitis and Ilargus). Although the predator to attack at close range, improving its chance both achieved a close colour match to litter from the per- of success (Elliott, McTaggart Cowan & Holling, 1977; spective of both prey and predators, Anasaitis spp. display Moore & Biewener, 2015). However, this strategy can be dis- highly contrasting stripes and a closer colour match to under- advantageous as sit-and-wait predators will have lower prey- storey foliage compared to Ilargus spp. As understorey foliage encounter rates than those that actively seek out prey represents a highly heterogenous background that is difficult (MacArthur & Pianka, 1966) and prey are able to scrutinise to colour-match, crypsis via disruptive colouration rather areas that might contain danger and subsequently change than background-matching is likely to benefit species that their trajectory if a predator is present. One solution is for occupy this . Furthermore, disruptive colouration is predators to use shelter to actively hide from prey. This is less background dependent, allowing predators to use a observed in trapdoor (family Ctenizidae) greater number of locations. This suggests that the (Leroy, 2003) and the shrimp (Lysiosquillina crypsis type adopted is likely driven most strongly by the loca- maculata) which usually ambush prey at night from burrows tion in which the predator forages. Camouflage via either (DeVries, Murphy & Patek, 2012). Others have hypothesised background-matching or a striking disruptive colouration is that predators such as (Panthera tigris) and also known in the wobbegong (family Orectolobidae) (Panthera pardus) primarily choose areas with high tree densi- (Compagno, Dando & Fowler, 2005; Huveneers, 2007). A ties to provide concealment from prey (Karanth & disruptive phenotype is achieved by a series of narrow longi- Sunquist, 2000). However, while this might reduce the risk tudinal flaps of along the side of the body that break up of detection by approaching prey, physical cover also could the body outline, together with a spotted body pattern reduce the predator’s ability to detect and track prey, whilst (Huveneers, 2007). This cryptic camouflage allows ambush acting as a barrier that makes the final capture more difficult. predation of a diverse range of prey (Ceccarelli & Thus, hiding behind physical features is likely only practised Williamson, 2012). Successful disruptive patterning is also by a minority of specialist ambush predators. known in species of orb-web spiders. Bright yellow banding It is perhaps because of these challenges that effective cam- on the dorsal abdominal surface of the orb-web spider Argiope ouflage is employed by many ambush predators. Ambush keyserlingi was found to have a cryptic function via disruptive predators are known to use mimetic to mislead colouration (Hoese et al., 2006). potential prey (Wickler, 1968; Ruxton et al., 2004) or cryptic Some predators have a flexible cryptic phenotype in which phenotypes to reduce initial detection, both of which ensure they can change their appearance in order to achieve a closer that prey move to within striking range. colour match to their background. For example, spiders (family Thomisidae) are able to change colour to match that of the specific flowers on which they hunt, to reduce detection (1) Aggressive crypsis by their hymenopteran prey and predators (Brechbuhl, As stated in Section I, one of the best-studied forms of cam- Casas & Bacher, 2010). Théry et al. (2005) compared the ouflage is background-matching. Its success as a mechanism chromatic contrast of a number of spiders and flowers to to avoid detection by predators or prey is dependent on the the detection thresholds of the spider’s prey () interaction between body colouration, the organism’s envi- and predators ( ), finding that in both visual ronment, and the observer’s (Merilaita, systems, the individual spider was able to match the precise Tuomi & Jormalainen, 1999; Stevens & Merilaita, 2009). colour of the flower. Some examples of background-matching in predators As well as background-matching via colour change, some appear to be used solely in order to reduce detection by prey. crab spiders use aggressive crypsis through decorative behav- For example, the levant lizard (Lacerta media israelica) has iour. The crab spiders Stephanopis scabra and S. cambridgei have a bright green colouration that is thought to function as cam- a high density of setae and tubercles on the body surface that ouflage in green vegetation (Disi et al., 2001). However, when facilitate attachment of pieces of tree bark as decoration

Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 4 Matilda Q. R. Pembury Smith and Graeme D. Ruxton

(Gawryszewski, 2014). Individuals with attached bark debris undetected until their prey is close enough for a successful were observed on bark with darker colours and individuals attack. They then inject them with saliva which causes instant without debris were found on lighter-coloured bark, in both paralysis. Prey that survive the initial attack will not be able to cases improving background-matching camouflage. flee, meaning that if the decoration limits their mobility, it is Previous studies have shown that the effectiveness of unlikely to impede prey-capture rate in this predator. background-matching and disruptive colouration is environ- In the examples described above, the success of the ment dependent (Price et al., 2019). Thus, these strategies masquerading phenotype is dependent on the surrounding may not be suitable for predators that capture prey in a environment. Some other ambush predators use a form of diverse range of habitat types. Transparency can be a suc- masquerade that reduces recognition in a range of environ- cessful form of camouflage that is less environmentally ments. Death feigning, well documented as an anti-predator dependent (Johnsen, 2001). This strategy has been documen- strategy by prey, has also been observed in predators. This ted mainly in prey organisms in pelagic environments, possi- behaviour is common amongst fish species bly because predators have a greater reliance on tissues such (Conkel, 1993; Tobler, 2005). McKaye (1981) reported that as muscle that are difficult to make transparent (McFall- the predatory cichlid Haplochromis livingstoni masquerades as Ngai & Montgomery, 1990; , Dilly & Cope, 2002). a dead fish by lying on its side semi-buried in the sand in Ingested prey will also increase predator visibility, as has order to ambush prey. Another predatory species of cichlid, been shown for transparent predatory Chaoborus sp. larvae livingstonii, matches the colour patterns of a fish (Giguère & Northcote, 1987). The siphonophores Agalma in the early stages of decay in order to attract small scaveng- okeni and Athorybia rosacea are highly transparent (back- ing fishes which attempt to feed on the corpse ground-matching), but they also have nematocyst batteries (McKaye, 1981). Field observations have also reported this which are not transparent and instead mimic the appearance behaviour in the comb (Mycteroperca acutirostris) (aggressive mimicry) of a and a larval fish, respec- (Gibran, 2004). tively. It is hypothesised that potential prey are attracted to Many species of frogfish are able to adopt a variety of phe- these mimetic parts (Purcell, 1980; Mackie, Pugh & notypes that allow them to masquerade in different environ- Purcell, 1987), allowing successful ambush by the ments. The striated frogfish ( striatus) has at least siphonophores. four distinct colour phases that allow it to masquerade as or as three different colours of (Pietsch & Grobecker, 1987). They change in colour as they move to dif- (2) Aggressive masquerade ferent , improving the efficiency of the masquerade. A ‘ in sheep’s clothing’ is an idiom used to describe dan- gerous individuals that appear harmless. This concept – (3) Aggressive mimicry termed ‘masquerade’–has been applied to predators that mimic an object in their environment to facilitate misidenti- Aggressive mimicry is a strategy in which a predator (the fication by prey (Skelhorn et al., 2010). For example, the ‘mimic’) simulates the properties of a ‘model’ to dupe poten- predatory orb-web spider Cyclosa ginnaga adds a white disc- tial prey (the ‘receiver’) in order to increase their shaped silk decoration to its web upon which it positions itself success (Wickler, 1968; Pasteur, 1982). This deceptive strat- to resemble a dropping (Skelhorn, 2015). This strategy egy is known in a variety of organisms including could have an anti-predatory function for the spider in addi- (Schiestel et al., 2003), and vertebrates tion to concealment from its own prey (Liu et al., 2014). Sim- (Pough, 1988; Sazima, 2002; Randall, 2005) and involves a ilarly, the South American fish Monocirrhus polyacanthus variety of sensory modalities. resembles a floating dead leaf as it approaches its prey As highlighted above, ambush predators are predicted to (Cott, 1940). Although this body , colour pattern have lower prey-encounter rates than active foragers and behaviour are likely used to facilitate predation (MacArthur & Pianka, 1966) since they must wait until prey (Catarino & Zuanon, 2010), it is unknown whether it also are in close proximity before they can attack. Perhaps provides protection from predators. because of this, many ambush predators display a beha- Masquerade via decoration will have associated costs: dec- vioural, physical or chemical lure to attract their prey. Many oration adds mass and hence may limit locomotory ability, aggressive mimics produce a generalised lure that mimics a making it most effective in predators that are predominantly broad class of model. However, as there is likely to be strong stationary. For example, assassin bugs of the genera Paredocla selection for lure effectiveness, natural selection has given rise and Acanthaspis cover their body with of their to lures that are species specific and exquisitely finely tuned. prey, dust, sand and soil particles using a sticky secretion as glue, to produce a protective ‘backpack’. The layer of dust (a) Aggressive mimicry without a lure has been shown to act as a chemical masquerade, specifically reducing the probability of detection by their prey, and the Many aggressive mimics have evolved a particular pheno- ant exoskeletons have been shown to reduce the risk of preda- type that allows them to approach or co-exist with their prey tion, as well as facilitating prey capture (Brandt & (Poulton, 1890). One well-known example is in the blue- Mahsberg, 2002). This masquerade allows them to remain striped fangblenny (Plagiotremus rhinorhynchos), which visually

Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Camouflage in predators 5 mimics juvenile blue-streaked cleaner (Labroides dimi- Grobecker, 1987), while that of the striated frogfish (A. striatus) diatus), allowing it to approach and feed off the scales of fishes resembles a bioluminescent worm (Brauwer & Hobbs, 2016). at cleaning stations (Cheney & Côté, 2005). The frogfish manipulates the lure in ways that simulate the Some organisms are able to combine multiple sensory natural swimming movements of the model. However, modalities to increase the efficiency of aggressive mimicry. despite each species displaying a unique lure, Pietsch & Gro- For example, common (Cuculus canorus) are nest par- becker (1987) found that the lures each attract a diverse vari- asites that lay eggs that match the colour and pattern of their ety of prey. ’s eggs (Honza et al., 2014; Li et al., 2016) to minimise the likelihood of host detection. After hatching, the nestlings also (c) Aggressive mimicry using a specialised lure mimic the begging sounds and behaviour of the host brood (Davies, Kilner & Noble, 1998; Stoddard & Stevens, 2010). Although there are many types of specialised aggressive mim- Similarly, the nestlings of the Horsfield’s bronze icry, perhaps the best documented is in which (Chalcites basalis) resemble the host nestlings both acoustically a predator uses a signal that mimics one of a specific prey and visually (Langmore et al., 2008, 2011). Another example species as a lure to attract (usually male) prey. For example, of aggressive mimicry involving multiple sensory modalities is the firefly versicolor lures male spp. fireflies provided by the zone-tailed hawk (Buteo albonotatus), which by mimicking the flashing courtship displays of the . has a clear resemblance with the turkey (Cathartes These flash–reply signals have a species-specific timing in aura). The prey of the zone-tail hawk are not predated by tur- relation to the courted male (Lloyd, 1975, 1984) and obser- key , making the vulture a suitable model. Zone- vational data have shown that Photuris versicolor is able to tailed hawks resemble turkey vultures in shape, colour and mimic up to 11 species-specific female ‘replies’. The genera flight behaviour, unlike other members of their . Photuris and Photinus are closely related, which perhaps Although the hawk is smaller than the vulture, they both fly explains the origin of their mimicry. at high altitudes which may make it difficult for prey to judge Species-specific signalling does not require close phyloge- their size accurately. This example of aggressive mimicry has netic relatedness. Marshall & Hill (2009) found that the pred- been suggested primarily to assist prey capture rather than atory katydid Chlorobalius leucoviridis can attract male provide a protective function (Willis, 1963). Similarly, it has (family Cicadidae) by imitating the species-specific wing-flick been suggested that the bird-eating bicolored hawk (Accipiter replies of sexually receptive female cicadas. This aggressive bicolor pileatus) is an aggressive mimic of the rufous-thighed mimicry is achieved both acoustically with terminal clicks, kite (Harpagus diodon) that preys on and and visually by using synchronised body jerks. Interestingly, (Cabanne & Roesler, 2007), but the evidence for this remains the katydids can mimic a variety of species-specific inconclusive (Amadon, 1961). songs which the predator has not encountered previously. Marshall & Hill (2009) proposed that this ability to mimic a broad range of songs has developed in C. leucoviridis by (b) Aggressive mimicry using a generalised lure exploiting the general design elements common in the songs One of the best examples of generalised aggressive mimicry is of many acoustically signalling insects that use duets in pair provided by the anglerfish (), which is a large formation. deep-water fish that preys on small predatory fish that, in The use of chemical signalling as a lure has also been docu- turn, prey on small invertebrates. Anglerfish possess a num- mented in aggressive mimicry systems. Female bolas spiders ber of spines that extend in front of the mouth and move to (Mastophora cornigera) attract male moth prey by mimicking mimic the behaviour of these prey while it three female moth sex [(Z)-9-tetradecenyl ace- remains stationary (Wilson, 1937; Pietsch & Grobecker, tate, (Z)-9-tetradecenal, and (Z)-11-hexadecenal] (Stowe, 1978). The behaviour mimicked is a generic behaviour dis- Tumlinson & Heath, 1987). The spiders prey on male moths played by multiple invertebrate prey. of at least 19 species. As a single blend of sex Similarly, the Australian crab spider (Thomisus spectablis) compounds is unlikely to attract all 19 moth species, Stowe has an (UV)-reflecting white carapace that makes et al. (1987) suggested that individual spiders may produce it conspicuous when sitting on UV-absorbing white flowers different blends of compounds to attract specific subsets of (Heiling, Herberstein & Chittka, 2003). This colour contrast prey. This would be an interesting avenue of research in has been shown to be conspicuous to a variety of hymenop- terms of the evolution of specialised chemical mimicry. teran prey, which appear to be attracted to the UV pattern- Specialised nutritional mimicry has also been documen- ing (Heiling et al., 2003, 2005a, b). ted, in which a predator mimics the prey species of the pred- Many species of frogfish also use a generalised lure. ator they are trying to capture. For example, some snakes Although frogfish species minimise detection through mas- remain predominantly motionless in a coiled position while querade (see Section II.2), many also use a mimetic lure to moving their tails in short ‘vermiform’ movements that entice prey to within striking distance. The shape and size resemble prey . Glaudas & Alexander (2017) showed of the lure are species specific. The lure of the hispid frogfish that puff adders (Bitis arietans) discriminate between prey (Antennarius hispidus) resembles a tube worm, that of the warty organisms and use specialised behaviour only frogfish (A. maculatus) resembles a small fish (Pietsch & against specific targets such as bufonid toads that prey on

Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 6 Matilda Q. R. Pembury Smith and Graeme D. Ruxton small moving objects. This clearly demonstrates that the sig- Barbosa et al., 2012) – and it allows predators nal can be specialised according to the environmental con- to achieve successful camouflage in a vast number of different text in which it is deployed. locations (Shohet et al., 2006; Zylinski et al., 2009). For exam- ple, the mimetic (Thaumoctopus mimicus) adopts a background-matching colouration when foraging for prey at low speeds. However, when moving faster, to capture III. PURSUIT PREDATORS moving prey or to escape their own predators, they adopt a body form that mimics other organisms in their environment, One of the most common strategies of predation is pursuit. such as swimming flatfish (Zebrias spp.), lionfish ( spp.) or Pursuit is any strategy that allows the predator to move closer banded snakes (Laticauda spp.). This switch in strategy is to its target. A predator may move towards prey rapidly by likely due to the limited success of background-matching chasing, or may approach stealthily until they are close when the organism is moving rapidly over a range of environ- enough to strike [stalking (Sunquist & Sunquist, 1989; Caro & ments. An in situ behavioural experiment using video and FitzGibbon, 1992)]. If the predator can reduce the prey’s image analysis (Josef et al., 2015) showed that, when moving ability to detect and/or identify it as a threat, this could allow between a black and background, the cuttlefish (Sepia a closer approach before the prey can deploy active counter- officinalis) changed their reflectance gradually in a sigmoidal measures (such as fleeing). manner to match the approaching background. To do this, However, previous studies show that movement tends to S. officinalis must estimate the time it will take to reach a break down camouflage (Scott-Samuel et al., 2011) as move- new background and the reflectance of the approaching ment produces a contrasting image against a stationary background, allowing it to maintain background-matching background (retinal slip) (Julesz, 1971; Regan & Beverley, camouflage during active pursuit of prey. The authors also 1984; Rushton, Bradshaw & Warren, 2007; Yin et al., found that the gradual change occurred primarily after the 2015; Mely et al., 2016) or reduces background-matching individual had moved onto the new background, meaning when organisms move between environments. As pursuit that there was a short period where crypsis was compro- predators rely on movement, they are likely to be at high risk mised. Although this suggests that dynamic camouflage of detection. requires time to integrate visual input and respond accord- Additionally, the also contains mov- ingly, in most natural environments clear transitions between ing elements. The physical movement of objects in the two backgrounds are rare, meaning that a gradual change (Ord et al., 2007; Peters, Hemmi & Zeil, 2007; New & may not provide a disadvantage to these individuals in Peters, 2010; Ryerson, 2017), underwater currents (Shohet the wild. et al., 2006), and dynamic patterns of light (Endler, 1993; Although background-matching may be less able to Endler & Théry, 1996) will affect a stationary predator’s reduce detection in moving individuals, this strategy may still ability to remain undetected. Although pursuit predators be favoured over other forms of crypsis. Zylinski et al. (2009) may be able to minimise detection by moving slowly towards compared cuttlefish body patterns used during movement or prey, successful capture may rely on a final high-speed when static against two background types, one of which attack. Predators are thus likely to experience a trade-off promoted a low-contrast mottled pattern and the other a between the ability to go undetected and movement that high-contrast disruptive pattern. Their results showed that allows successful prey capture. It is of interest, therefore, to high-contrast body patterns were not used during motion as consider how camouflage can be achieved in moving organ- these increased detection against a background of small, isms in dynamic environments (Rushton et al., 2007; Hall moving particles in coastal waters. Thus, for moving cuttle- et al., 2013). fish, a background-matchinglow-contrast pattern was more effective than disruptive crypsis. (1) Dynamic crypsis via background-matching fi The ef ciency of many cryptic strategies relies on minimal (2) Dynamic crypsis via disruptive colouration movement against an unchanging background. Camouflage through background-matching will clearly be reduced in Crypsis via disruptive patterning is common across a wide dynamic individuals, although slow movement may minimise range of taxa. This reduces detection by breaking up the the detectability of actively moving individuals with a body outline (Merilaita, 1998). Allen et al. (2011) investigated background-matching phenotype. have been background-matching patterns in felids and found that the used as model organisms for analysing dynamic camouflag- spotted pattern of the (Acinonyx jubatus), serval (Caracal ing as they can assess complex visual scenes and produce a serval) and black-footed cat (Felis nigripes) contrasts greatly with body pattern that matches their surroundings (Zylinski, their open habitat. They suggested that this pattern reduces Osorio & Shohet, 2009). This background-matching is detection by prey via disruption. leopards (Panthera achieved by – cytoplastic sacs of unica) display disruptive colouration with a white coat pat- controlled by motor neurons attached to radial muscles terned with irregular dark grey rosettes and spots. The result- (Marshall & Messenger, 1996; Mäthger & Hanlon, 2006; ing coat, with highly contrasting patches of colour, breaks up

Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Camouflage in predators 7 the body outline to achieve camouflage in their mountain Gordon, 1997), group movement has also been shown to environment (McCarthy & Chapron, 2003). reduce the ability of an observer to track moving individuals: Disruptive colouration provides concealment from prey ‘the confusion effect’ (Krakauer, 1995). The confusion effect when predators are stationary, moving slowly (stalking) or coupled with a disruptive phenotype could provide a selec- moving quickly (chasing). Highly contrasting and disruptive tive advantage in group-living predators. For example, patterns have also been shown to alter an observer’s percep- Hogan et al. (2017) found that artificial prey targets with tion of the speed and trajectory of moving objects (Thayer, stripes parallel to their direction of movement impeded the 1909; Stevens et al., 2008; Scott-Samuelet al., 2011; Hughes, tracking of one target among many, and that this effect inter- Troscianko & Stevens, 2014; Hall et al., 2016; Hogan, Cut- acted positively with increases in group size. This process hill & Scott-Samuel, 2017). This has been described as could benefit group-hunting predators, such as the spotted ‘motion dazzle’ camouflage (Hogan, Cuthill & Scott- hyena (Crocuta crocuta) (Watts & Holekamp, 2007), by reduc- Samuel, 2016a, b). For example, Scott-Samuelet al. (2011) ing the ability of prey to determine predator trajectories suc- showed that dazzle-patterned objects can be perceived as cessfully, thus increasing the likelihood of interception. moving more slowly than plain objects. This has also been Despite this, for predators to capture prey they need to iden- tested with predatory mantids, showing that prey with nar- tify, target and pursue a single individual. By contrast, prey row stripes are harder for mantids to detect than those with only need to detect a generic predator to initiate anti- a background-matching pattern. This is thought to be predator behaviours. Thus, selection pressures for tracking because a striped pattern blurs into a single colour when prey individuals within a group are likely to be stronger in preda- are in motion, allowing them to blend into the background tors than in prey. (Umeton et al., 2019). By contrast, prey with a background- matching phenotype containing dark and light areas become (3) Motion masquerade more conspicuous when moving. Such patterns require a fas- ter movement speed before they appear a uniform colour, The motion of background elements is universal in natural compared with a narrow-stripe pattern. It is therefore likely environments, both randomly or in a directed that predators with disruptive patterns could achieve benefits (e.g. moving water, wind motion of or the movement both by minimising detection and by disrupting speed per- of other organisms). Ease of detection in an environment is ception (Stevens et al., 2008, 2011; Scott-Samuelet al., 2011; affected by the signal-to-noise ratio (SNR). SNR is a balance Hughes et al., 2014; Hämäläinen et al., 2015; Hughes, between useful and irrelevant information where the signal is Magor-Elliott & Stevens, 2015). By reducing the ability of the target and the noise involves all factors that interfere with prey to detect the direction or speed of an attack, disruptive the target’s detection and identification (Merilaita phenotypes will minimise the ability of prey to escape suc- et al., 2017). As a result, for prey to locate a moving predator cessfully. Supporting evidence for this idea has been provided they must discriminate between predator movement by Santer, (2013) using locust prey and a series of digital pat- (dynamic signal) and irrelevant moving objects in the envi- to simulate the approach of a predator from distances ronment (dynamic noise). ranging from 0.07 to 10 m away. Locusts have a pair of des- Light movement in the environment affects camouflage in cending contralateral movement detector (DCMD) neurons terrestrial and aquatic predators. In aquatic , light allowing them to respond rapidly to objects moving towards will pass through the surface of the water and refract. This, them. Santer (2013) showed that high-contrast patterns pro- coupled with moving ripples or , leads to rapid changes duce a weak DCMD response in the locust, leading to in the areas that are exposed to light (Lock & Andrews, 1992; delayed escape behaviour. This suggests that predators with Swirski et al., 2009), potentially revealing the location of high-contrast colour patterns may be at an advantage as this camouflaged organisms. Light is thus a source of visual noise phenotype will minimise detection by prey. Similar tests car- that can affect detection (Ortolani & Caro, 1996; ried out on tasked with targeting moving digital Ortolani, 1999; Allen et al., 2011; Merilaita et al., 2017). images (Troscianko et al., 2008) found that organisms with Selection for a phenotype that minimises the effects of light conspicuous patterns (such as stripes and zigzags) were more was hypothesised by Merilaita & Stevens et al. (2011), who difficult to capture than uniformly coloured individuals suggested that dwarf whales (Kogia sima) and minke whales (Stevens et al., 2008; Hughes et al., 2014). (Balaenoptera acutorostrata) have undulating dorsoventral The complexity of motion-dazzle camouflage increases for contrasting-colouration stripes in order to background- animals that live in groups. Group membership and group match changing light conditions. Similarly, analyses by Orto- movement is seen widely throughout the animal kingdom lani & Caro (1996), Ortolani (1999) and Allen et al. (2011) (Krause & Ruxton, 2002). Although this behaviour has been showed that predatory cats living in forested environments documented as an anti-predator strategy (Stevens et al., are more likely to have complex colour patterns than those 2011), some predators also move as a group to hunt and cap- in open habitats. These closed environments have more ture prey (Bednarz, 1988; Packer & Ruttan, 1988; Creel & irregular and complex elements, dense vegetation and high Creel, 1995; Kitchen & Packer, 1999). Although group hunt- levels of light dappling, which produce high-contrast ing may increase the size of prey that can be subdued or shadows (Endler, 1993). The observed coat patterns conse- reduce levels of (Carbone, DuToit & quently mimic the effects of light dappling and shadow

Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 8 Matilda Q. R. Pembury Smith and Graeme D. Ruxton production, potentially reducing detection of moving preda- tors by prey, although this has yet to be demonstrated. Most documented responses to variation in light to reduce detection are behavioural. One study on the behaviour of the white (Carcharodon carcharias) found that they position themselves along an east–west axis from morning to after- noon on sunny days to keep the sun behind them while they are hunting, as this will reduce detection by exploiting sur- face sun glare (Heveneers et al., 2015). This strategy both reduces the amount of direct sunlight in the of the predator and illuminates the prey they are trying to catch. Further studies on this species showed that attack frequencies on Cape seals (Arctocephalus pusillus) are highest at high lunar and low sunlight illumination (Fallows, Fallows & Hammerschlag, 2016). Both situations will produce a silhou- ette of their prey at the water surface whilst the sharks remain camouflaged against dark water. Fig 1 Illustration of two forms of predator pursuit. X is the starting point of the predator; Y is the starting point of the prey; both are moving to the right of the page. Classical (4) Motion camouflage pursuit is where the predator directly follows the position of the moving prey. Deviated pure pursuit is where the predator Intercepting a moving target relies on a predator modifying moves in a direction that maintains a constant angle to the its trajectory by anticipating the movement of their prey final intercept position of the target. This follows the constant (Anderson & McOwan, 2003a). The optimal path for the bearing, decreasing range (CBDR) principle and the success of predator is thus not always the one that directs the predator this strategy will be facilitated by motion camouflage (see Fig. 2). to the current location of the prey, but rather towards a potential interception point of their two future trajectories. produce the same image motion on the of another Some organisms capture prey via classical pursuit, in which animal (the shadowee) as would a stationary object in the the predator directly follows the path of the moving prey environment.” This could allow successful concealment (Kramer, 2001) (Fig. 1). However, this is only possible if the against both homogenous and structured backgrounds predator is faster than its prey (Moore & Biewener, 2015). (Srinivasan & Davey, 1995) and data show that motion cam- An alternative is to follow a trajectory that can be predicted ouflage via this mechanism can result in a more energy- and by the proportional navigation model, the basis of which fol- time-efficient pursuit path compared to classical pursuit lows the ‘constant bearing, decreasing range’ (CBDR) or (Glendinning, 2004; Troscianko et al., 2008). ‘deviated pure pursuit’ concept (Fig. 1). In this strategy, the Srinivasan & Davey (1995) have proposed a series of algo- predator will move in a straight line, maintaining a constant rithms to describe motion-camouflage trajectories. The bearing relative to a predicted intercept position with the predator chooses a particular object or some point to use as moving prey while closing the distance between them, even- a ‘fixed point’ (F; see Fig. 2A). If the predator moves along tually to intercept it (Murtaugh & Criel, 1966) (Fig. 1). To use a line connecting F and the prey (the ‘camouflage constraint this method successfully, capture requires the pursuing indi- line’; see Fig. 2A), this will create the impression that the vidual to predict the intersection of its own trajectory with predator is stationary at F as the prey will perceive no lateral that of the target. Robots with biologically plausible inputs motion (retinal slip) as the predator approaches (Troscianko have successfully carried out deviated pure pursuit without et al., 2008). For example, if the predator starts its approach the entire trajectory being known at the onset (Rañó & towards the prey in front of a rock, by maintaining a position Iglesias, 2016) and computation modelling studies have directly between the rock and the current position of the shown that organisms can successfully intercept moving tar- prey, the optic flow of the predator projected onto the retina gets via CBDR by predicting trajectories (Anderson & of the prey would mean the predator would appear to be sta- McOwan, 2003b). This method of target interception has tionary against the rock (Anderson & McOwan, 2003b). By been demonstrated in dogs (Shaffer et al., 2004), fish using this strategy, motion camouflage could conceal the (Lanchester & Mark, 1975), (Ghose et al., 2006) and predator’s movement (Srinivasan & Davey, 1995). Although humans (Fajen & Warren, 2004). the predator will appear to increase in size, this change in size Predators must also be able to manoeuvre towards a mov- will be hard to detect, allowing the predator to close its dis- ing target whilst minimising their own probability of detec- tance to the prey (Anderson & McOwan, 2002). tion. Motion camouflage may use the CBDR concept This method can also allow a predator to appear as a sta- whilst minimising detection by using the perceived motion tionary landmark without the presence of an object to use as of elements in the optic field. Mizutani, Chahl & Sriniva- a fixed point as long as the predator remains on the camou- san (2003, p. 604) describe motion camouflage as when flage constraint line. If the predator can estimate distance “one animal (the shadower) moves in such a way as to p from any fixed point F and distance d from the prey (see

Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Camouflage in predators 9

Fig 2 Illustration of motion camouflage. (A) Trajectories of a predator (X) and prey (Y). This motion trajectory gives the impression that predator X is a stationary object at point F, behind the actual position of the predator. (B) In order to appear consistently at the initial position of pursuit (F), the predator must calculate the angle DO and adjust its lateral movement by distance DI by estimating its distance from F (p) and its distance from the prey (d). Figures adapted from Srinivasan & Davey (1995).

Fig. 2B), it can camouflage its motion by (i) always viewing constraint line (Fig. 2). Although this does not mean that the prey frontally, (ii) pointing radially away from F, and the predator will reach the prey in the shortest time, it does (iii) making appropriate changes in angle D0 and distance allow the predator to approach without detection. However, D1 (Fig. 2B). To carry out this method of motion camouflage pursuit that costs the predator more time and/or energy will successfully both DI and D0 must be estimated accurately, reduce the net worth of the prey, thus potentially reducing requiring the predator to be able to make rapid predictions the motivation of the predator to initiate an attack regarding future prey movements. Two- and three- (Krebs, 1980). Furthermore, over evolutionary timescales dimensional computer have shown that artificial natural selection may have led prey to adopt unpredictable predators can approach prey successfully by predicting their trajectories to make it more difficult for a predator to move future movements using simple input data (Anderson & along the camouflage constraint line. Srinivasan & McOwan, 2003b), thus achieving motion camouflage by Davey (1995) emphasise that their model is based on many appearing to remain stationary. Srinivasan & Davey (1995) simplifying assumptions that may only apply under certain tested their model using data collected by Collett & circumstances due to the complexity of predator–prey inter- Land (1978) on hoverfly (family Syrphidae) flight actions (Curio, 1976). Such models may provide insights into paths and found that they moved such that the shadower’s other motion camouflage mechanisms, and perhaps facilitate motion was along the camouflage line, providing evidence the development of new military or security applications. that these algorithms are applicable to biological systems. Motion camouflage behaviour may be particularly applica- ble to dragonflies as they have a highly sophisticated neural cir- IV. FACTORS AFFECTING THE EVOLUTION OF cuit that allows detection of moving objects against a moving STRATEGIES IN PREDATORS background (Mizutani et al., 2003). Recent data show that fal- cons (Falco spp.) also use cues from prey movement to determine flight direction. Video data showed that approach prey (1) Time of attack at a constant angle, following a flight path that fits the predic- The unpredictability of predatory attacks means that prey tions of motion camouflage behaviour (Kane & Zamani, 2014). should benefit from continual expression of traits that reduce The successful use of motion camouflage dictates that a detection by predators. As pursuit predators determine the predator is constrained to move along the camouflage onset of an attack, unlike in prey, there will be less selection

Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 10 Matilda Q. R. Pembury Smith and Graeme D. Ruxton for a continuously camouflaged phenotype. Thus, beha- camouflage in predators still await experimental investiga- vioural camouflage techniques that minimise movement tion, making it an important avenue for future research. detection are likely to be selected for in pursuit predators, The success of motion-dazzle camouflage is also likely to with strategies which rely on continuous background- be affected by size. Murali & Kodandaramaiah (2016) inves- matching being less common, since camouflage is not neces- tigated the effect of stripe patterns and size on attack rates in sary during non-hunting periods. Despite this prediction, lizards. They found that the presence of a longitudinal stripe cryptic camouflage is observed in pursuit predators, suggest- redirected attacks to the lizard’s tail by exploiting the motion- ing it does provide a benefit in some species. However, dazzle effect. In later work, Murali & Kodandara- whether this is to facilitate prey capture or an adaptation maiah (2018) also demonstrated that this benefit was greater against their own predators remains unclear. for shorter lizards. As a relationship between body size and In aggressive mimicry and cryptic strategies, predators can the effects of patterning has also been found in snakes show finely tuned traits that may maximise their chances of (Allen et al., 2013), it was hypothesised that smaller prey ani- successful ambush, such as species-specific deceptive signals mals benefit more from the known effects of high-contrast or accurate cryptic or masquerading phenotypes (Nelson, patterns on perceived speed and motion dazzle (Hall Garnett & Evans, 2010; Bartos, Szczepko & Stanska, 2013). et al., 2016; Murali & Kodandaramaiah, 2016). As larger Jackson & Wilcox (1993) showed that web-invading jumping organisms have reduced manoeuvrability (Webb, 1983), it spiders ( spp.) display an array of different deceptive sig- is possible that increasing body size reduces the selective nals and monitor feedback from their spider prey. Following advantage of this type of camouflage; indeed, in the absence such feedback, the predator produces only the signal that eli- of erratic movements, this form of camouflage could make cited a positive response. By using this method, the spider can them more conspicuous (Hogan et al., 2016b). Conceivably identify species-specific signals with which to fine-tune its therefore, predator size also could be a factor influencing aggressive mimicry in order to capture a diverse range of the evolution of camouflage strategies in pursuit predators. prey. By contrast, prey organisms can only anticipate the risk Camouflage strategies found in ambush predators are also of predation to a degree, and have limited control over what affected by size. For organisms that use aggressive mimicry or type of predator attacks them and when. This means that aggressive masquerade, their body size and shape will deter- prey need to retain a wide range of defensive traits to protect mine which models they can successfully resemble. For them from many types of predator, and over a range of differ- aggressive mimics that use a lure resembling the prey or ent environmental contexts. opposite sex of the prey, the size of the predator will poten- tially impact the success of the mimetic phenotype. Evidence for this can be seen in organisms that display ‘transformation ’ (2) Size mimicry ; wherein they change to mimic different models during their life, in tandem with changes in body size and Predators must be large and strong enough to subdue their shape. For example, the mantis species Mantoida maya mimics prey, particularly when the prey are mobile and able to an ant species when young and small, and a species of fl ee. Previous studies have shown that size can affect detect- when it is older and larger (Jackson & Drummond, 1974). ability even when stationary, with larger animals being more easily detected (Mänd, Tammaru & Mappes, 2007; Remmel & Tammaru, 2009; Karpestam, Merilaita & (3) Prey Forsman, 2014) and hence it may be harder for larger Broom & Ruxton (2005) hypothesised that two optimal prey fl organisms to achieve effective camou age. For example, strategies are likely to occur: prey will either flee immediately Cuadrado, Martin & Lopez (2001) investigated the cryptic when the predator is detected (before the predator has begun success of (Chamaeleo chamaeleon) by investigat- an attack) or will only flee in response to a direct attack. ing detection rate by predators in relation to size and back- Although their model focuses on optimal strategies for prey, fi ground in photographs and in the eld. The probability of it can be used to investigate the circumstances under which fi detection was size dependent, with detection time signi - certain strategies may be selected. For cantly shorter for larger chameleons. As well as affecting example, the relative frequency with which these strategies fl detection, body size in uenced the distance from an are used depends on a range of different conditions. The approaching predator at which the chameleons initiated strategy of fleeing as soon as a predator becomes visible is escape. Smaller individuals allowed closer approach dis- associated with slow predator search speed, low energetic tances than larger individuals (Cuadrado et al., 2001). Sim- cost to in prey, large advantages to prey if they are ilar size-dependent retreat behaviour has been recorded in the first to move, limited ability by prey to detect the predator other prey species (Heatwole, 1968; Burger & Gochfeld, at a distance, high ability to detect prey by the predator, and 1990; Martín & Lopez, 1995). high probability that the predator will be successful if a chase We can subsequently hypothesise that detection of move- occurs. Under these conditions, therefore, there may be ment in pursuit predators is likely to be size dependent, with selection for predators to evolve strategies such as motion larger predators potentially having to initiate an attack when masquerade or crypsis to minimise the likelihood that prey they are further away. However, the effects of size on will flee before the predator has initiated a chase. By contrast,

Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Camouflage in predators 11 where prey only flee in response to a direct attack, motion experimentally varied the parasite load in staghorn damsel- camouflage or motion dazzle may be selected for, as this will fish (Amblyglyphidodon curacao) and observed changes in forag- reduce the ability of prey to detect the true speed, direction ing success of an aggressive mimic (the bluestriped or trajectory of a direct attack. However, such predictions fangblenny) of the bluestreak cleaner . When parasite remain speculative. Future research modelling optimal pred- loads were increased, the attack success of the fangblennies ator strategies is needed to understand how prey drive the also increased as there was a greater cost to the damselfish evolution of camouflage in pursuit predators. from avoiding cleaning stations. Thus, we can hypothesise Prey group size is also likely to affect selection on pursuit that there will be selection on prey to detect signals associated predators that rely on delayed detection by prey. As prey with predators, however this will be offset by the potential group size increases, the probability of predator detection loss of feeding or breeding opportunities. increases (Pulliam, 1973; Elgar & Catterall, 1981) due to The costs associated with learned avoidance are likely to the benefits of shared vigilance. As a result, predators that differ depending on whether the predator uses aggressive target group-living prey will be under stronger selection to mimicry, aggressive masquerade or aggressive crypsis. There minimise detection before initiating pursuit (Kenward, is likely to be a lower cost associated with avoiding objects or 1978; Fitzgibbon, 1989). In addition to increased prey vigi- other organisms used in aggressive masquerade/crypsis than lance, large group sizes could reduce predator success by a with avoiding food or a potential mate to minimise predation greater confusion effect of more moving targets, thereby risk. As a result, learned avoidance may evolve more easily in reducing a predator’s ability to track one individual success- response to some types of crypsis in comparison to others. fully (Krakauer, 1995). It is likely, therefore, that predators Attack success in ambush predation depends on a number hunting group-living prey will be under strong selection for of variables including habitat structure (Whittingham & strategies that aid successful interception and the ability to Evans, 2004) and prey group size (Fitzgibbon, 1989; Dever- track specific individuals in a moving group. eux et al., 2006). However, when prey misidentify a mimetic Defensive mimicry has been the subject of much research. sit-and-wait predator as an unthreatening model – and the The two best-known examples are , in predator is then successful – the prey organism does not sur- which palatable mimics resemble unpalatable models vive. This potentially means that there will be strong selection (Bates, 1862; Lea & Turner, 1972), and Müllerian mimicry, for avoidance behaviour in prey over evolutionary time- in which multiple unpalatable species converge on a spe- scales. Future research should focus on how the type of cific colour pattern to enhance the value of the aposematic aggressive mimicry affects the evolution of avoidance behav- signal of unpalatability (Müller, 1879). Both types of mim- iour as well as investigating long-term changes in aggressive icry are subject to frequency-dependent selection. As a mimicry systems. Batesian mimic becomes more common in the population, The selection pressures driving aggressive mimicry, the fitness of this phenotype decreases as predators are aggressive masquerade or aggressive crypsis are likely to more likely to correctly identify that they are palatable. involve context- and prey-dependenttrade-offs. For example, For Müllerian mimics, as mimic frequency increases the lure-based aggressive mimicry reduces predator energy fitness of the phenotype will increase as their predators will expenditure as it relies on manipulating prey to approach. correctly identify particular mimics and learn to avoid However, prey scrutiny is likely to be higher, as the signal them (Cheney & Côté, 2005). Ings & Chittka (2009) found draws attention to the location of the predator. By contrast, that exposed to a random mixture of yellow in aggressive masquerade, crypsis or mimicry without a lure, and white flowers, in which some of the yellow flowers prey are not actively attracted towards the predator, making contained ‘robotic’ crab spiders, learned to avoid the yel- them less likely to be identified, although the prey-encounter low flowers regardless of whether the crab spider was rate will also be lower. As a result, the best strategy for an present. is likely to be affected by prey type. Preda- Although learnt avoidance is seen in aggressive mimics, it tors that catch many different types of prey may be more will not affect them in the same way as defensive mimics. likely to use aggressive masquerade or crypsis, to maximise As signal-based aggressive mimics use models that benefit their ability to be inconspicuous. Specific aggressive mimicry prey organisms, a prey organism that learns to avoid a poten- is likely to be more beneficial when a predator is limited to tial mate or food item will have lower survival or reproduc- specific prey types. tion. Thus, the selection pressures for learnt avoidance are In lure-based aggressive mimicry, the two most common likely to differ in aggressive mimicry systems. This has been types of lure are sexual or nutritional. Although there has observed in the bluestriped fangblenny/juvenile cleaner been limited focus on predators, we can analyse preferences wrasse aggressive mimicry system (see Sections II.3a). for certain types of lure in other biological systems, such as Cleaner fish display mutualistic relationships with many reef pollination. Orchids provide an example of deceptive fish species, benefiting their clients by removing parasites and flowers, with around one-third of all species offering no dead skin, which they use as a food source. By mimicking rewards to pollinators (Jersakova, Johnson & Kindlmann, them, the fangblenny is able to reach close proximity with 2006), instead attracting them by using food or sexual decep- the reef fish, but then attacks them by biting off pieces of their tion (Dafni, 1983; Nilsson, 1983; Fritz, 1990; Schiestl, 2005). flesh (Johnson & Hull, 2006). Côté & Cheney (2007) production is energetically expensive (Southwick,

Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 12 Matilda Q. R. Pembury Smith and Graeme D. Ruxton

1984) so adaptations that allow pollination without having to minimised learnt avoidance by reef fish. Mimic success also provide a reward may be under positive selection. The same increased with the population density of other fish on the argument can be applied to predators: any trait that increases reef, suggesting that ‘victim’ frequency dependence could predator–prey encounter rate while minimising costs such as affect the evolution of aggressive mimicry. Further investi- energy expenditure could be subject to positive selection, as gations into the selective forces underlying aggressive mim- seen in the evolution of lures. icry systems will help us to understand the mechanisms Different lures may have different associated costs, affect- behind their maintenance. ing their evolution. In ambush predator–prey systems, the A predator’s position in the may also drive dif- success of a signal is likely to be prey dependent. Nutritional ferent selection for camouflage strategies. Non-apex preda- lures may be selected in predators that prey on organisms tors are themselves subject to predation, leading to selection that have a low or low diversity of food sources, for anti-predator adaptations. For example, apex predators and hence a higher cost to avoidance behaviour. Reproduc- may be more likely to evolve motion camouflage as they tive lures may only be effective at certain times of the year are not under selection for camouflage other than during where the mimicked species breeds seasonally (Tauber, Tau- an attack. By contrast, predators lower in the food chain ber & Masaki, 1986). There is also some evidence for learned may be under selection for strategies that reduce detection avoidance towards sexual mimics (DeJager & Ellis, 2014), by their own predators (e.g. crypsis or masquerade). This and that capacity is influenced by the ratio of models could include the expression of different behaviours depend- to mimics (Ferdy et al., 1998). Subsequently, as described ing on whether they are actively trying to capture prey or to above for Batesian mimicry, this system will be frequency avoid predation. Similarly in many s, an odour is released to dependent. mimic a model chemically as well as visually (Haynes et al., 2002). This may have the disadvantage of alerting the mimic’s own predators and may be selected against in non- (4) Environment apex ambush predators. Phenotypic trade-offs in pursuit predators are likely to affect Although an interesting avenue for future research would the selection for certain camouflage strategies. There are be to investigate the relationship between a predator’s posi- documented cases of trade-offs between a camouflaged tion in the food chain and their camouflage strategy, distin- appearance and a different colour pattern with another pri- guishing whether strategies have evolved in order to mary function (e.g. thermoregulation or sexual signalling) minimise predator detection or increase prey capture may (Stuart-Foxet al., 2008). Although such trade-offs have only be challenging. Recently, new technologies such as drones been investigated to date in prey (Norris & Milstead, 1967; and biologging have emerged that allow continuous observa- Hemmi et al., 2006), there is no reason to suggest that pursuit tions of wild predators over large spatial and temporal scales predators would not be subject to similar trade-offs. If a (Wich & Koh, 2018), and effective monitoring in the labora- camouflaged phenotype disadvantages a predator in some tory using camera equipment and virtual or robotic prey. For way (whether thermoregulatory or sexually), selection is example, Ioannou et al. (2019) used simulations of virtual likely to lead to strategies that are only expressed under spe- prey with real predators in order to assess differential preda- cific circumstances (e.g. motion camouflage, motion mas- tion risk experienced by individuals within a group depend- querade and dynamic crypsis). It could be hypothesised that ing on their social role. Similarly, Pietsch & where predators receive a benefit from conspicuous colours Grobecker (1990) analysed the biomechanics of feeding in or patterns (e.g. in ), they may be under strong three species of frogfish (A. striatus, A. hispidus and selection for disruptive phenotypes, to allow distortion of A. maculatus) by integrating frame-by-frame analysis of high- speed and direction estimation by prey while still conferring speed film with anatomical analysis of the bones, muscles mating success. and ligaments in the head. One of the defining features of mimicry is that the mimic affects the selection pressures experienced by the model and vice versa. Thus model frequency will affect the evolution of mimetic phenotypes in ambush predators. There is only lim- V. CONCLUSIONS ited work on how frequency dependence affects the evolution of aggressive mimicry systems (Davies, 2000; Kunze & (1) Although camouflage is predominantly thought of as an Gumbert, 2001). One interesting series of investigations anti-predator defence mechanism, many unique strategies involves the bluestriped fangblenny and the juvenile cleaner are also observed in predators, and those expressed in both wrasse (see Sections II.3a and IV.3) (Randall, Allen & groups are likely to be driven by different selective forces. Steene, 1997; Côté & Cheney, 2004, 2007; Cheney & Côté, (2) In ambush predators, three main strategies have 2005). Cheney & Côté (2005) showed that this mimicry sys- evolved that act to minimise the prey’s ability to detect or tem was affected by the relative frequencies of the mimic, identify the predator before an attack: aggressive mimicry the model and the potential victims. The number of success- (which may involve a generalised or specialised lure), aggres- ful attacks was higher when the predatory mimics were rel- sive masquerade, and aggressive crypsis. In pursuit preda- atively rare compared to their mutualistic model, as this tors, four main strategies have evolved that minimise the

Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Camouflage in predators 13 prey’s ability to detect or identify the predator: motion cam- BRAUWER,M.D.& HOBBS,J.A.(2016). Stars and stripes: biofluorescent lures in the fl striated frogfish indicate role in aggressive mimicry. Coral Reefs 35, 1171. ou age, motion masquerade and dynamic crypsis via- BRECHBUHL,R., CASAS,J.& BACHER,S.(2010). Ineffective crypsis in a crab spider: a background-matching or disruptive camouflage. prey perspective. Proceedings of the Royal Society B: Biological Sciences 277, (3) Two evolutionary explanations for camouflage differ- 739–746. BROOM,M.& RUXTON,G.D.(2005). You can run-or you can hide: optimal strategies ences between predators and prey are the ability of predators for cryptic prey against pursuit predators. 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(Received 2 January 2020; revised 24 April 2020; accepted 28 April 2020)

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